Oxidized lipids block antigen cross-presentation by dendritic cells in cancer

Journal of Immunology

Volumn 192, Issue 6, 2014, Pages 2920-2931

  Cao, Wei ^a   Ramakrishnan, Rupal ^a   Tuyrin, Vladimir A ^b   Veglia, Filippo ^c   Condamine, Thomas ^c   Amoscato, Andrew ^a   Mohammadyani, Dariush ^d   Johnson, Joseph J ^a   Zhang, Lan Min ^a   Klein Seetharaman, Judith ^e   Celis, Esteban ^a   Kagan, Valerian E ^b   Gabrilovich, Dmitry I ^a,c  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c WISTAR INSTITUTE   (United States)

^d University of Pittsburgh   (United States)

^e UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHOLESTEROL ESTER; FATTY ACID; GROWTH FACTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEINASE; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR CD204; TRIACYLGLYCEROL; TUMOR DERIVED FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; CELL POPULATION; CELL SURFACE; COLON CARCINOMA; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; LEWIS CARCINOMA; LIPID OXIDATION; MELANOMA; MOUSE; NEOPLASM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL LINE;

ACETYLCYSTEINE; ANIMALS; ANTIGEN PRESENTATION; CELL LINE, TUMOR; CELLS, CULTURED; CROSS-PRIMING; CULTURE MEDIA, CONDITIONED; CYSTEINE PROTEINASE INHIBITORS; DENDRITIC CELLS; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTERFERON-GAMMA; LIPIDS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NEOPLASMS; OVALBUMIN; OXIDATION-REDUCTION; PEPTIDE FRAGMENTS;

EID: 84897506146     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302801     Document Type: Article

References (52)

1. Hildner, K., B. T. Edelson, W. E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B. U. Schraml, E. R. Unanue, M. S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322: 1097-1100.
2. Knight, S. C., S. Iqball, M. S. Roberts, S. Macatonia, and P. A. Bedford. 1998. Transfer of antigen between dendritic cells in the stimulation of primary T cell proliferation. Eur. J. Immunol. 28: 1636-1644.
3. Yewdall, A. W., S. B. Drutman, F. Jinwala, K. S. Bahjat, and N. Bhardwaj. 2010. CD8+ T cell priming by dendritic cell vaccines requires antigen transfer to endogenous antigen presenting cells. PLoS ONE 5: e11144.
4. Gabrilovich, D. I., S. Ostrand-Rosenberg, and V. Bronte. 2012. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12: 253-268.
5. Ascierto, P. A., M. Napolitano, E. Celentano, E. Simeone, G. Gentilcore, A. Daponte, M. Capone, C. Caracò, R. Calemma, G. Beneduce, et al. 2010. Regulatory T cell frequency in patients with melanoma with different disease stage and course, and modulating effects of high-dose interferon-alpha 2b treatment. J. Transl. Med. 8: 76.
6. Yigit, R., C. G. Figdor, P. L. Zusterzeel, J. M. Pots, R. Torensma, and L. F. Massuger. 2011. Cytokine analysis as a tool to understand tumour-host interaction in ovarian cancer. Eur. J. Cancer 47: 1883-1889.
7. Yamagami, W., N. Susumu, H. Tanaka, A. Hirasawa, K. Banno, N. Suzuki, H. Tsuda, K. Tsukazaki, and D. Aoki. 2011. Immunofluorescence-detected infiltration of CD4+FOXP3+ regulatory T cells is relevant to the prognosis of patients with endometrial cancer. Int. J. Gynecol. Cancer 21: 1628-1634.
8. Shen, X., N. Li, H. Li, T. Zhang, F. Wang, and Q. Li. 2010. Increased prevalence of regulatory T cells in the tumor microenvironment and its correlation with TNM stage of hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 136: 1745-1754.
9. Bevan, M. J. 1976. Minor H antigens introduced on H-2 different stimulating cells cross-react at the cytotoxic T cell level during in vivo priming. J. Immunol. 117: 2233-2238.
10. Bevan, M. J. 1976. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143: 1283-1288.
11. Burgdorf, S., and C. Kurts. 2008. Endocytosis mechanisms and the cell biology of antigen presentation. Curr. Opin. Immunol. 20: 89-95.
12. Joffre, O. P., E. Segura, A. Savina, and S. Amigorena. 2012. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12: 557-569.
13. Alvarez, D., E. H. Vollmann, and U. H. von Andrian. 2008. Mechanisms and consequences of dendritic cell migration. Immunity 29: 325-342.
14. McDonnell, A. M., A. C. Prosser, I. van Bruggen, B.W. Robinson, and A. J. Currie. 2010. CD8alpha+ DC are not the sole subset cross-presenting cell-associated tumor antigens from a solid tumor. Eur. J. Immunol. 40: 1617-1627.
15. van Mierlo, G. J., Z. F. Boonman, H.M. Dumortier, A. T. den Boer, M. F. Fransen, J. Nouta, E. I. van der Voort, R. Offringa, R. E. Toes, and C. J. Melief. 2004. Activation of dendritic cells that cross-present tumor-derived antigen licenses CD8+ CTL to cause tumor eradication. J. Immunol. 173: 6753-6759.
16. Gerner, M. Y., K. A. Casey, and M. F. Mescher. 2008. Defective MHC class II presentation by dendritic cells limits CD4 T cell help for antitumor CD8 T cell responses. J. Immunol. 181: 155-164.
17. Engelhardt, J. J., B. Boldajipour, P. Beemiller, P. Pandurangi, C. Sorensen, Z. Werb, M. Egeblad, and M. F. Krummel. 2012. Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells. Cancer Cell 21: 402-417.
18. Perrot, I., D. Blanchard, N. Freymond, S. Isaac, B. Guibert, Y. Pachéco, and S. Lebecque. 2007. Dendritic cells infiltrating human non-small cell lung cancer are blocked at immature stage. J. Immunol. 178: 2763-2769.
19. Gabrilovich, D. I. 2004. Mechanisms and functional significance of tumourinduced dendritic-cell defects. Nat. Rev. Immunol. 4: 941-952.
20. Melief, C. J. 2008. Cancer immunotherapy by dendritic cells. Immunity 29: 372-383.
21. Preynat-Seauve, O., P. Schuler, E. Contassot, F. Beermann, B. Huard, and L. E. French. 2006. Tumor-infiltrating dendritic cells are potent antigen-presenting cells able to activate T cells and mediate tumor rejection. J. Immunol. 176: 61-67.
22. Wakim, L. M., and M. J. Bevan. 2011. Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection. Nature 471: 629-632.
23. Dolan, B. P., K. D. Gibbs, Jr., and S. Ostrand-Rosenberg. 2006. Dendritic cells cross-dressed with peptide MHC class I complexes prime CD8+ T cells. J. Immunol. 177: 6018-6024.
24. Bougnères, L., J. Helft, S. Tiwari, P. Vargas, B. H. Chang, L. Chan, L. Campisi, G. Lauvau, S. Hugues, P. Kumar, et al. 2009. A role for lipid bodies in the crosspresentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31: 232-244.
25. Saka, H. A., and R. Valdivia. 2012. Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu. Rev. Cell Dev. Biol. 28: 411-437.
26. Walther, T. C., and R. V. Farese, Jr. 2012. Lipid droplets and cellular lipid metabolism. Annu. Rev. Biochem. 81: 687-714.
27. Herber, D. L., W. Cao, Y. Nefedova, S. V. Novitskiy, S. Nagaraj, V. A. Tyurin, A. Corzo, H. I. Cho, E. Celis, B. Lennox, et al. 2010. Lipid accumulation and dendritic cell dysfunction in cancer. Nat. Med. 16: 880-886.
28. Zhou, J., P. Cheng, J. I. Youn, M. J. Cotter, and D. I. Gabrilovich. 2009. Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30: 845-859.
29. Remily-Wood, E. R., R. Z. Liu, Y. Xiang, Y. Chen, C. E. Thomas, N. Rajyaguru, L. M. Kaufman, J. E. Ochoa, L. Hazlehurst, J. Pinilla-Ibarz, et al. 2011. A database of reaction monitoring mass spectrometry assays for elucidating therapeutic response in cancer. Proteomics Clin. Appl. 5: 383-396.
30. Folch, J., M. Lees, and G. H. Sloan Stanley. 1957. A simple method for the isolation and purification of total lipides from animal tissue. J. Biol. Chem. 226: 497-509.
31. Overwijk, W. W., A. Tsung, K. R. Irvine, M. R. Parkhurst, T. J. Goletz, K. Tsung, M. W. Carroll, C. Liu, B. Moss, S. A. Rosenberg, and N. P. Restifo. 1998. gp100/pmel 17 is a murine tumor rejection antigen: induction of "self"-reactive, tumoricidal T cells using high-affinity, altered peptide ligand. J. Exp. Med. 188: 277-286.
32. Bieghs, V., F. Verheyen, P. J. van Gorp, T. Hendrikx, K. Wouters, D. Lütjohann, M. J. Gijbels, M. Febbraio, C. J. Binder, M. H. Hofker, and R. Shiri-Sverdlov. 2012. Internalization of modified lipids by CD36 and SR-A leads to hepatic inflammation and lysosomal cholesterol storage in Kupffer cells. PLoS ONE 7: e34378.
33. Tyurina, Y. Y., V. A. Tyurin, A. A. Shvedova, J. P. Fabisiak, and V. E. Kagan. 2002. Peroxidation of phosphatidylserine in mechanisms of apoptotic signaling. Methods Enzymol. 352: 159-174.
34. Tsuchiya, M., V. E. Kagan, H. J. Freisleben, M. Manabe, and L. Packer. 1994. Antioxidant activity of alpha-tocopherol, beta-carotene, and ubiquinol in membranes: cis-parinaric acid-incorporated liposomes. Methods Enzymol. 234: 371-383.
35. Burgdorf, S., C. Schö lz, A. Kautz, R. Tampé, and C. Kurts. 2008. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9: 558-566.
36. Platt, N., and S. Gordon. 2001. Is the class A macrophage scavenger receptor (SR-A) multifunctional? - The mouse's tale. J. Clin. Invest. 108: 649-654.
37. Wang, X. Y., J. Facciponte, X. Chen, J. R. Subjeck, and E. A. Repasky. 2007. Scavenger receptor-A negatively regulates antitumor immunity. Cancer Res. 67: 4996-5002.
38. Aliberti, J., S. Hieny, C. Reis e Sousa, C. N. Serhan, and A. Sher. 2002. Lipoxinmediated inhibition of IL-12 production by DCs: a mechanism for regulation of microbial immunity. Nat. Immunol. 3: 76-82.
39. Weatherill, A. R., J. Y. Lee, L. Zhao, D. G. Lemay, H. S. Youn, and D. H. Hwang. 2005. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J. Immunol. 174: 5390-5397.
40. Shamshiev, A. T., F. Ampenberger, B. Ernst, L. Rohrer, B. J. Marsland, and M. Kopf. 2007. Dyslipidemia inhibits Toll-like receptor-induced activation of CD8alpha-negative dendritic cells and protective Th1 type immunity. J. Exp. Med. 204: 441-452.
41. Angeli, V., J. Llodrá, J. X. Rong, K. Satoh, S. Ishii, T. Shimizu, E. A. Fisher, and G. J. Randolph. 2004. Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 21: 561-574.
42. van Manen, H.-J., Y. M. Kraan, D. Roos, and C. Otto. 2005. Single-cell Raman and fluorescence microscopy reveal the association of lipid bodies with phagosomes in leukocytes. Proc. Natl. Acad. Sci. USA 102: 10159-10164.
43. Tyurin, V. A., W. Cao, Y. Y. Tyurina, D. I. Gabrilovich, and V. E. Kagan. 2011. Mass-spectrometric characterization of peroxidized and hydrolyzed lipids in plasma and dendritic cells of tumor-bearing animals. Biochem. Biophys. Res. Commun. 413: 149-153.
44. Zaguri, R., I. Verbovetski, M. Atallah, U. Trahtemberg, A. Krispin, E. Nahari, E. Leitersdorf, and D. Mevorach. 2007. 'Danger' effect of low-density lipoprotein (LDL) and oxidized LDL on human immature dendritic cells. Clin. Exp. Immunol. 149: 543-552.
45. Jensen, P. E. 2007. Recent advances in antigen processing and presentation. Nat. Immunol. 8: 1041-1048.
46. Touret, N., P. Paroutis, M. Terebiznik, R. E. Harrison, S. Trombetta, M. Pypaert, A. Chow, A. Jiang, J. Shaw, C. Yip, et al. 2005. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123: 157-170.
47. Basha, G., G. Lizée, A. T. Reinicke, R. P. Seipp, K. D. Omilusik, and W. A. Jefferies. 2008. MHC class I endosomal and lysosomal trafficking coincides with exogenous antigen loading in dendritic cells. PLoS ONE 3: e3247.
48. Lizée, G., G. Basha, J. Tiong, J. P. Julien, M. Tian, K. E. Biron, and W. A. Jefferies. 2003. Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat. Immunol. 4: 1065-1073.
49. Gagnon, E., S. Duclos, C. Rondeau, E. Chevet, P. H. Cameron, O. Steele-Mortimer, J. Paiement, J. J. Bergeron, and M. Desjardins. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110: 119-131.
50. Basha, G., K. Omilusik, A. Chavez-Steenbock, A. T. Reinicke, N. Lack, K. B. Choi, and W. A. Jefferies. 2012. A CD74-dependent MHC class I endolysosomal cross-presentation pathway. Nat. Immunol. 13: 237-245.
51. Al Gadban, M. M., K. J. Smith, F. Soodavar, C. Piansay, C. Chassereau, W. O. Twal, R. L. Klein, G. Virella, M. F. Lopes-Virella, and S. M. Hammad. 2010. Differential trafficking of oxidized LDL and oxidized LDL immune complexes in macrophages: impact on oxidative stress. PLoS ONE 5: e12534.
52. Mohammadyani, D., V. A. Tyurn, A. A. Amoscato, D. I. Gabrilovich, J. Klein-Seetharaman, and V. E. Kagan. 2014. Computational approaches to understanding the role of oxidized tri-aclyglycerols in suppression of antigen crosspresentation in cancer. Biophys. J. 106: 805a-806a.